Protozoan–bacterial symbiosis in a deep‐sea hydrothermal vent folliculinid ciliate (Folliculinopsis sp.) from the Juan de Fuca Ridge

Abstract

This study provides a first description of the morphology of Blue Mats: sessile, colonial folliculinid ciliates (Folliculinopsis sp.) that create dense bright blue carpets in certain Juan de Fuca Ridge vent fields and at vents elsewhere. In one area of widespread venting, for example, Blue Mats occupied approximately 70% of the substratum. The ultrastructure of the Blue Mat ciliates was investigated in samples from Axial Volcano on the Juan de Fuca Ridge using conventional scanning electron microscopy and thin section transmission electron microscopy. These Folliculinopsis sp. ciliates secrete and dwell in tubes (loricae). The loricae were colonized by both coccoid and filamentous bacteria‐like structures. Greater densities of coccoid‐ and short‐rod‐shaped bacteria were found between rows of cilia on the ciliate body (zooid) and especially on the peristomal lobes (arm‐like extensions typical to folliculinid ciliates). A coccoid bacterial morphotype (within and independent of a vacuole) was located throughout the ciliate cytoplasm. Groups of this organism clustered within vacuoles were regularly distributed along the ciliate cortex. Electron dense, vacuole‐bound features characterized by stacked membranous structures were also found within the ciliate cytoplasm. These results suggest the existence of at least an endosymbiosis between Folliculinopsis sp. ciliates and bacteria at hydrothermal vents. The chemolithoautotrophic nature of these symbiotic bacteria remains to be confirmed. To our knowledge, this is the first report of a protozoan–bacterial symbiosis at vents, as well as the first reported symbiosis in folliculinid ciliates.

Blue mats: faunal composition and food web structure in colonial ciliate (Folliculinopsis sp.) mats at Northeast Pacific hydrothermal vents

“…These ciliate mats can cover extensive areas on basalt surfaces or patches on sulfide chimneys in some eastern Pacific Ocean hydrothermal vent fields and elsewhere (Tunnicliffe et al 1985, Kouris et al 2007). For example, in areas of widespread venting of 10 to 20 m 2 or more on the Juan de Fuca Ridge, blue mats occupied as much as 70% of the basaltic substratum (Kouris et al 2007). At some vent sites, these folliculinid ciliates have also been reported attached to mobile invertebrates (Kouris et al 2007), as well as on the tubes of the vestimentiferan Ridgeia piscesae (Bergquist et al 2007, Gollner et al 2007).…”

Diversity of invertebrate colonists on simple and complex substrates at hydrothermal vents on the Juan de Fuca Ridge

“…This scale of complexity can be found in the natural environment within tightly woven Ridgeia piscesae tubeworm bushes (Tsurumi & Tunnicliffe 2003) or the dense colonies of folliculinid ciliates, Folliculinopsis sp. ('blue mat'; Kouris et al 2007). The faunal assemblages that colonized sponge substrates had higher abundance, diversity and evenness than assemblages that colonized the basalt substrates.…”

“…The tubes of vestimentiferans and shells of bivalves provide a complex structure that is inhabited by smaller vent invertebrates (Govenar et al 2002, 2005, Van Dover 2002, 2003, Tsurumi & Tunnicliffe 2003, Bergquist et al 2007). On the Juan de Fuca Ridge, northeastern Pacific, small-scale (millimetres to centimetres) spatial habitat complexity is also provided by sessile colonial folliculinid ciliates ('blue mat') that secrete and dwell within chitinous tubes of 0.3 to 2 mm in length (Kouris et al 2007). These tubes attach to the basalt substratum and onto each other, creating dense colonies that can cover ~70% of the available surface area at diffuse vents.…”

Colonial Tube-Dwelling Ciliates Influence Methane Cycling and Microbial Diversity within Methane Seep Ecosystems

“…A sister clade of methanotrophs ("Deep sea-1") includes known symbionts of a few seep and vent marine invertebrate taxa (e.g., Cavanaugh et al, 1987;Schmaljohann et al, 1990;DeChaine and Cavanaugh, 2006;Wendeberg et al, 2012) as well as a ciliate from a lowoxygen environment (Edgcomb et al, 2011). The vent-associated folliculinids were reported to have intracellular microorganisms that were morphologically similar to methanotrophs (Kouris et al, 2007), however, morphology alone was not able to confirm whether these features were methanotrophs or pigmented granules.…”

“…These ciliates are found in non-chemosynthetic coastal marine habitats (e.g., Fauré-Fremiet, 1936;Das, 1949;Mathews, 1964Mathews, , 1968Ji et al, 2004) and are known to colonize a variety of substrates including oyster and mussel shells (Mathews, 1968;Toupoint et al, 2012), serpulid polychaete worm tubes (Mathews, 1964), crayfish (Jaszczolt and Szaniawsk, 2007), wood (Mathews, 1964), coral skeletons (Cróquer et al, 2006), and even artificial substrates (Ji et al, 2004). Their presence in chemosynthetic ecosystems was first discovered at hydrothermal vents in the 1980's (Tunnicliffe et al, 1985;Van Dover et al, 1988), but their abundance and ecological importance was only more recently recognized (Kouris et al, 2007(Kouris et al, , 2010. Folliculinids form dense "blue mat" colonies within hydrothermal vent fields, sometimes occupying 70% of mineralized substrate, influencing community composition and food web structure within these ecosystems (Kouris et al, 2010).…”